BEACON Researchers at Work: How the cricket lost its song

This week’s BEACON Researchers at Work post is by MSU postdoc Robin Tinghitella.

Photo of Robin TinghitellaLast April I had the pleasure of writing the very first BEACON Researchers at Work blog post. I shared a story about how a tropical field cricket, Teleogryllus oceanicus, hitchhiked from Australia (where they’re native) through the Pacific, colonizing island after island, until they finally reached the Hawaiian Islands.  It’s a great story about how humans can drive biological evolution because the crickets probably traveled on canoes with Polynesian settlers as they themselves island-hopped through the Pacific during the Polynesian expansion. For an evolutionary biologist like myself, the really intriguing part of the story is what happened once the crickets arrived in Hawaii. As a family friend announced during my wedding ceremony, the Hawaiian crickets lost their “chirpedness.” In other words, a rare mutation wiped out their ability to sing to attract mates. But how could that possibly work?

Graphic representation of founder's effect

Figure 1

When organisms colonize new environments, rapid evolutionary change frequently follows. This is primarily because of two things: genetic bottlenecks and novel selection pressures. Genetic bottlenecks happen when the size of a population is drastically reduced by chance. Large populations are typically made up of lots of different types of individuals with different characteristics. In other words, they have high genetic diversity. But when a chance event happens, the individuals who live on to reproduce may not represent all of the types that were found in the original population, many genes can be lost in the process, and the genetic diversity ends up being much, much lower. When organisms colonize new locations, the same type of thing happens. Founding populations are typically made up of very few individuals who don’t necessarily represent all of the genetic diversity present in their source populations (Figure 1). This makes a lot of sense when you think about something as drastic as colonizing islands like Hawaii. Hawaii is 2000 miles from the nearest Pacific island – how many individuals would you expect to arrive there by floating on flotsam, being carried on wind gusts or hitching a ride on a canoe? My guess is not very many. In the case of the tropical field crickets, the trip across the Pacific serves as the “bottleneck” through which only a few individuals make it. Once founders arrive in a new location, they face a whole host of challenges in their new environments – novel selection pressures – things that may not have existed in their source ranges and that may favor very different characteristics than those that were advantageous in their original habitats.

Back to the tropical field crickets, then. Crickets are a classic study system for biologists who are interested in sexual signals, things like bird plumage and frog calls that are typically used by males to attract females. Even Darwin was puzzled by these sorts of showy, exaggerated traits precisely because they are so conspicuous and seem to defy natural selection. Crickets are a great model system for this sort of work because males produce two songs that are used in mating contexts – first, they sing a calling song (a long distance, high intensity song) to attract females from afar. Females are the locomotory sex, so they move through the environment (grassy fields) in search of singing males. Once they are in close proximity, males switch to producing a quiet courtship song. Both songs are thought to be required before a female will mate with a male and mating is entirely under the control of the female – it’s a classic “female choice” system in which males cannot coerce females into mating. Females even have more subtle preferences for certain aspects of the song (like the length of certain parts of the song or what proportion of singing time is filled with sound (the duty cycle)) that they use to decide which males they will mate with.  In any event, the songs are really conspicuous and like many sexual signals, they often attract the attention of unintended receivers, things like predators and parasites that instead use these mating signals to locate potential hosts and prey. In Hawaii, T. oceanicus encounters a novel natural enemy that exists nowhere else in its range – it’s a parasitoid fly called Ormia ochracea that uses the crickets’ mating song to locate hosts for their maggots to live off of.

Photo of parasitoid larvae in cricket

Figure 2

In an alien-like plot, this fly has drastically changed the way the crickets locate mates on two islands in Hawaii. Pregnant female flies locate signaling males and spray larvae on and around them, some of which will burrow into the body cavity of the cricket where they’ll spend the next 7-10 days literally eating the cricket from the inside out (Figure 2 – photo by J.T. Rotenberry). Hawaiian T. oceanicus, then, face a conflict between natural and sexual selection. They should sing to locate females, but singing is very risky. What happened next in Hawaii was a surprise to those of us who study this system – the crickets just stopped singing.

Photos of normal and flatwing males

Figure 3

After several months of scratching our heads, we put the pieces of the puzzle together. The crickets had a rare mutation that we called “flatwing”. The mutation changes their wing morphology in a way that eliminates their ability to sing to attract mates. Male crickets typically sing using specialized ridged structures on the wings, but flatwing males are missing all of those structures (Figure 3), so they’re physically incapable of producing the songs that crickets are so well known for. The flatwing mutation probably originally appeared in just one or very few individuals, but it spread through the population to 95% of males on the island of Kauai in fewer than 20 generations. That’s one of the fastest recorded evolutionary shifts in a wild population! This discovery led to so many questions: Why did the mutation spread so quickly? What’s the advantage to being a flatwing male over a calling male? If you already guessed that flatwing crickets avoid being parasitized by the fly, you’re right. We dissected over 120 flatwing males and only one of them was parasitized. That’s a far cry from the >35% parasitization rates that were found on Kauai before the mutation appeared.

But even if flatwing crickets are safe from the fly, the rest of the story still doesn’t make sense. Silent crickets should be really unsuccessful when it comes to mating (males use song to locate females and t
o “convince” them to mate), so a mutation like flatwing shouldn’t be passed on to future generations. Yet this mutation spread like wildfire and there’s a thriving population of almost all silent crickets on Kauai. How do males and females find each other without the use of song? And, why do females mate with them? These questions made up the bulk of my dissertation research, and what I discovered has inspired my subsequent work to answer a basic question about female mating decisions: “why that guy?”

It turns out that male crickets sometimes use an alternative mating behavior called satellite behavior to locate mates. Instead of calling themselves, satellite males hang out near singing males and attempt to intercept females who have been attracted to the other guys. Lots of organisms like frogs, toads, and insects that signal acoustically sometimes use satellite behavior. The advantage is that satellites can avoid the energetic costs of producing songs or calls as well as the risk (of predation or parasitization) associated with singing or calling themselves. Check out this cartoon that explains how satellite behavior works. In Hawaii, flatwings behave as satellites to the remaining 5% or so of males who can call. The flies can’t find the flatwings, but flatwing males can still manage to find females! What’s more, we found out that satellite behavior existed as a behavioral option for males before the change in wing morphology. Regardless of their wing morphology, males seem to use satellite behavior most when they haven’t mated recently. We can imagine that might happen anytime the population density is low or the competition for mates is stiff. What’s really cool about this is that is suggests pre-existing behavior facilitated the loss of song, so maybe behavior plays an important role in rapid evolution. Without satellite behavior silent males couldn’t find mates and flatwing males wouldn’t have passed their flatwing genes on to future generations.

Photo of Robin Tinghitella

Robin "surfing" on Hawaii

Satellite behavior gets us as far as males and females finding each other, but it still doesn’t explain why females are willing to mate with a male who can’t produce the sexual signal. Past research tells us that females clearly have strong preferences, even requirements, for hearing the courtship song before mounting males for mating. Let’s think back to the very first females who colonized the Hawaiian populations of T. oceanicus to see if they can help us reason this out. Recall that the vast open ocean between Hawaii and the nearest land serves as a bottleneck that only a few crickets made it through to colonize the Hawaiian Islands. The small initial population size may also have contributed to the spread of the flatwing trait. Imagine you’re a female cricket and you land on an island somewhere in the Pacific with not very many mates to choose from. If you’re extremely choosy you may never find an acceptable mate, which means the end of your genetic line. In other words, small founding populations may favor (select for) females who are lax in their mating decisions. In mating trials with females from across the crickets’ range (Australia, Oceania, and Hawaii) we found that females from Hawaii, and Kauai in particular, were the least choosy – they mate with silent flatwing males 50% of the time whereas females from Western Australia accept them only <10% of the time. So, the process of island colonization seems to have primed the Hawaiian populations for this rapid evolutionary change. The unfussy females allowed the mutation to take hold and spread on Kauai. In another location, like Australia, even if the mutation occurred, it may not have spread because picky females would not have accepted silent flatwing males as mates. So, again, it seems we found a special role for behavior in rapid evolution. And now I have a bit more information with which to answer the question, “why that guy?”

The papers I’ve covered in this post are:

Tinghitella, R.M. & Zuk, M. 2009. Asymmetric mating preferences accommodated the rapid evolutionary loss of a sexual signal. Evolution. 63: 2087-2098.

Tinghitella, R.M., Wang, J.M.* & Zuk, M. 2009. Pre-existing behavior renders a mutation adaptive: flexibility in male phonotaxis and the loss of singing ability in the cricket Teleogryllus oceanicus. Behavioral Ecology. 20: 722-728.

Zuk, M., Rotenberry, J.T. & Tinghitella, R.M. 2006. Silent Night: Adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biology Letters. 2: 521-524.

For more information about Robin’s work, you can contact her at hibbsr at msu dot edu.

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